Environmental Science and Pollution Research

, Volume 26, Issue 2, pp 1435–1444 | Cite as

In situ genotoxicity assessment in freshwater zooplankton and sediments from different dams, ponds, and temporary rivers in Tunisia

  • Zouhour Ouanes-Ben OthmenEmail author
  • Sabria Barka
  • Zied Ben Adeljelil
  • Samia Mouelhi
  • Mounira Krifa
  • Soumaya Kilani
  • Leila Chekir-Ghedira
  • Joëlle Forget-Leray
  • Amel Hamza-Chaffai
Research Article


Tunisia water resources are limited. The country currently has 29 large dams, more than 1000 hill lakes, and 220 small dams which are essential for economic and social development given their contribution to irrigation, drinking water consumption, flooding protection, production of electrical energy, groundwater recharge, and industrial uses. Given the scarcity of these resources, it is crucial to be able to ensure the quality of freshwater environments, particularly those intended for human consumption. In this study, we meant to assess the health status of various freshwater ecosystems in different regions of Tunisia (north and center west) in order to detect genotoxic components in sediments and their potential effect on zooplankton (cladocerans). Sediment and cladoceran species were collected from dams, ponds, and temporary rivers in Tunisia. For each collection site, micronucleus (MN) assay was performed, in triplicates, using a pool of ten specimens of the same cladoceran species. MN occurrence in cladocerans varied from one site to another and MN frequencies varied between 0.67 and 22‰, suggesting the presence of genotoxic substances in certain sites. Sediment genotoxicity and mutagenicity were assessed using the SOS Chromotest and the Ames test. Sediment results showed that genotoxicity varies from one site to another displaying a quantitative and a qualitative variation of pollutant among the sites. These results suggest an urgent need for continuous monitoring of freshwater environments in Tunisia, particularly those intended for drinking water.


Micronucleus assay Cladocerans Freshwater zooplankton Genotoxicity and mutagenicity assessment Ames test SOS Chromotest 



The authors wish to thank Soukeyna Mhedhbi and Karima Ltaief for their helpful technical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ayari J, Arfaoui M, Loukil C, Ouirou M (2012) Impact d’un site minier abandonné sur l’environnement : cas de la mine de Khanguet Kef Ettout (la région de Nefza), 17ème Colloque international en évaluation environnementale, 12–15 juin 2012, MontréalGoogle Scholar
  2. Barka S, Ouanes Z, Gharbi A, Gdara I, Mouelhi S, Hamza-Chaffai A (2016) Monitoring genotoxicity in freshwater microcrustaceans: a new application of the micronucleus assay. Mut Res 803–804:27–33CrossRefGoogle Scholar
  3. Bejaoui Kefi B, Latrous El Atrache L, Kochkar H, Ghorbel A (2011) TiO2 nanotubes as solid-phase extraction adsorbent for the determination of polycyclic aromatic hydrocarbons in environmental water samples. J Environ Sci 23:860–867CrossRefGoogle Scholar
  4. Bouhlel S (2007) Les ressources en plomb, zinc, fer, argent, cuivre, or , barytine, fluorine et célestite de la Tunisie : un bilan de 117 ans de recherches, d’explorations et d’exploitations, XVIIèmes Journées Nationales de la SSNT November 03–06, HammametGoogle Scholar
  5. Bour A, Mouchet F, Cadarsi S, Silvestre J, Baqué D, Gauthier L, Pinelli E (2017) CeO2 nanoparticle fate in environmental conditions and toxicity on a freshwater predator species: a microcosm study. Environ Sci Pollut Res 24:17081–17089CrossRefGoogle Scholar
  6. Burdon RH (2003) The suffering gene: environmental threats to our health. Zed books Ltd, New York, p 255Google Scholar
  7. Cachot J, Geffard O, Augagneur S, Lacroix S, Le Menach K, Peluhet L, Couteau J, Denier X, Devier MH, Pottier D, Budzinski H (2006) Evidence of genotoxicity related to high PAH content of sediments in the upper part of the Seine estuary (Normandy, France). Aquat Toxicol 79:257–267CrossRefGoogle Scholar
  8. Camargo JA (2003) Fluoride toxicity to aquatic organisms: a review. Chemosphere 50:251–264CrossRefGoogle Scholar
  9. Carver JH, Hatch FT, Branscomb EW (1979) Estimating maximum limits to mutagenic potency from cytotoxic potency. Nature 279:154–156CrossRefGoogle Scholar
  10. Carver JH, Mitchell AD, Waters MD (1983) Relationship(s) between mutation and cytotoxicity induced in vitro. In: Waters MD, Sandhu SS, Lewtas J, Claxton L, Chernoff N, Nesnow S (eds) Short-term bioassays in the analysis of complex environmental mixtures III. environmental science research, vol 27. Springer, Boston, pp 229–244Google Scholar
  11. Casellato S, Del Piero S, Masiero L, Covre V (2013) Fluoride toxicity and its effects on gametogenesis in the aquatic oligochaete Branchiura sowerbyi Beddard. Res Rep Fluoride 46:7–18Google Scholar
  12. Chapman D (1996) Water quality assessments a guide to the use of biota, sediments and water in environmental monitoring. Chapman and Hall Ltd, London, p 651Google Scholar
  13. Chen G, White P (2004) The mutagenic hazards of aquatic sediments: a review. Mutat Res 567:151–226CrossRefGoogle Scholar
  14. Chouchane H, Hoekstra AY, Krol MS, Mekonnen MM (2015) The water footprint of Tunisia from an economic perspective. Ecol Indic 52:311–319CrossRefGoogle Scholar
  15. COPEAU, European Program for “Control Web for pollution monitoring of water in Tunisia” (2009) Bull Sem Inform sur la Qualité de l’Eau, 3:8–9Google Scholar
  16. Dave G, Aspegren P (2010) Comparative toxicity of leachates from 52 textiles to Daphnia magna. Ecotoxicol Environ Saf 73(7):1629–1632Google Scholar
  17. Erciyas K, Sarikaya R (2010) Genotoxic evaluation of sodium fluoride in the somatic mutation and recombination test (SMART). Food Chem Toxicol 47:2860–2862CrossRefGoogle Scholar
  18. Fenech M, Bonassi S, Turner J, Lando C, Ceppi M, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Bigatti MP, Bolognesi C, Cao J, De Luca G, Di Giorgio M, Ferguson LR, Fucic A, Garcia Lima O, Hadjidekova VV, Hrelia P, Jaworska A, Joksic G, Krishnaja AP, Lee YK, Martelli A, McKay MJ, Migliore L, Mirkova E, Müller WU, Odagiri Y, Orsiere T, Scarf MR, Silva MJ, Sofuni T, Suralles J, Trenta G, Vorobtsova I, Vral A, Zijno A (2003) Intra- and inter-laboratory variation in the scoring of micronuclei and nucleoplasmic bridges in binucleated human lymphocytes results of an international slide-scoring exercise by the HUMN project. Mutat Res 534:45–64CrossRefGoogle Scholar
  19. Goswami P, Thirunavukkarasu S, Godhantaraman N, Munuswamy N (2014) Monitoring of genotoxicity in marine zooplankton induced by toxic metals in Ennore estuary, southeast coast of India. Mar Poll Bull 88:70–80CrossRefGoogle Scholar
  20. Houde M, Douville M, Gagnon P, Sproull J, Cloutier F (2015) Exposure of Daphnia magna to trichloroethylene (TCE) and vinyl chloride (VC): evaluation of gene transcription, cellular activity, and life-history parameters. Ecotoxicol Environ Saf 116:10–18CrossRefGoogle Scholar
  21. Jdid A, Blazy P, Kamoun S, Guedria A, Marouf B, Kitane S (1999) Environmental impact of mining activity on the pollution of the Medjerda River, north-west Tunisia. Bull Eng Geol Env 57:273–280CrossRefGoogle Scholar
  22. Jha AN (2004) Genotoxicological studies in aquatic organisms: an overview. Mutat Res Genet Toxicol Environ Mutagen 552:1–17CrossRefGoogle Scholar
  23. Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scale oxide particles. Environ Pollut 157:1619–1625CrossRefGoogle Scholar
  24. Jolibois B, Guerbet M (2005) Evaluation of industrial, hospital and domestic wastewater genotoxicity with the Salmonella fluctuation test and the SOS Chromotest. Mutat Res Genet Toxicol Environ Mutagen 565:151–162CrossRefGoogle Scholar
  25. Klobucar G, Pavlica M, Erben R, Papes D (2003) Application of the micronucleus and comet assays to mussel Dreissena polymorpha haemocytes for genotoxicity monitoring of freshwater environments. Aquat Toxicol 64:15–23CrossRefGoogle Scholar
  26. Koçak E, Yetilmezsoy K, Gonullu MT, Petek M (2010) A statistical evaluation of the potential genotoxic activity in the surface waters of the Golden Horn Estuary. Mar Pollut Bull 60:1708–1717CrossRefGoogle Scholar
  27. Korbaa M, Bejaoui M, Boumaiza M (2009) Spatio-temporal variation of the structure of the ephemeropterofauna in Sejnane stream (Ichkeul, northern Tunisia). Rev Sci Eau 22:373–381Google Scholar
  28. Kreijl CF, Slooff W (1985) Mutagenic activity in Dutch river waters and its biological significance for fish. In: Zimmerman FK, Taylor-Mayer RE (eds) Mutagenicity testing in environmental pollution control. Horwood, London, pp 63–68Google Scholar
  29. Lacaze E, Devaux A, Mons R, Bony S, Garric J, Geffard A, Geffard O (2011) DNA damage in caged Gammarus fossarum amphipods: a tool for freshwater genotoxicity assessment. Environ Pollut 159:1682–1691CrossRefGoogle Scholar
  30. Li HH, Aubrecht J, Fornace AJ (2007) Toxicogenomics: overview and potential applications for the study of non-covalent DNA interacting chemicals. Mutat Res Fund Mol Mutag 623:98–108CrossRefGoogle Scholar
  31. Mansour M, Tarhouni J (2012) Etude qualitative de la retenue Sejnane (identification de l’origine des matières en suspension et du fer). Mémoire de Master, INAT, Tunisia, p 52Google Scholar
  32. Margaritora FG (1985) Cladocera, Fauna d’Italia 23, Calderini, Bologna, p 399Google Scholar
  33. Maron D, Ames BN (1983) Revised methods for the Salmonella mutagenicity test. Mut Res 113:173–215CrossRefGoogle Scholar
  34. Maruoka S, Yamasaki S, Yamamoto Y (1986) Isolation of mutagenic components by high-performance liquid chromatography from XAD extract of water from the Nishitakase River, Kyoto City, Japan. Sci Total Environ 57:29–38CrossRefGoogle Scholar
  35. Marvin CH, McCarry BE, Villella J, Allan LM, Bryant DW (2000) Chemical and biological profiles of sediments as indicators of sources of genotoxic contamination in Hamilton Harbour: part I. Analysis of polycyclic aromatic hydrocarbons and thia-arene compounds. Chemosphere 41:979–988CrossRefGoogle Scholar
  36. Marzougui A, Ben Mammou A (2006) The Sejnane dam : silting quantification and valuation of specific erosion of its catchment area. Geo Eco Trop 30:57–68Google Scholar
  37. Massoud MA, Scrimshawa MD, Lester JN (2003) Qualitative assessment of the effectiveness of the Mediterranean action plan: wastewater management in the Mediterranean region. Ocean Coast Manag 46:875–899CrossRefGoogle Scholar
  38. Meireles G, Abe F, Accoroni K, Zanoni M, Oliveira D (2014) The commercial textile dye disperse red 73 induces toxicity in Danio rerio and Daphnia similis. Toxicol Lett 229:S112CrossRefGoogle Scholar
  39. Metcalfe-Smith JL, Holtze KE, Sirota GR, Reid JJ, de Solla SR (2003) Toxicity of aqueous and sediment-associated fluoride to freshwater organisms. Environ Toxicol Chem 22:161–166CrossRefGoogle Scholar
  40. Mlayah A, Ferreira da Silva EA, Hatira N, Jellali S, Lachaal F, Charef A, Noronha F, Ben Hamza C (2011) The Oued Serrat: mining activity, ground water and dispersion of base metals in natural environments (North-Western Tunisia). Rev Sci Eau 24:159–175Google Scholar
  41. Morry DW, Steinmaus C (2011) Evidence of the carcinogenicity of fluoride and its salts. Reproductive and Cancer Hazard Assessment Branch Office of Environmental Health Hazard Assessment. California Environmental Protection Agency, USA, p 22Google Scholar
  42. Ochoa-Herrera V, Banihani Q, Leon G, Khatri C, Field JA, Sierra-Alvarez R (2009) Toxicity of fluoride to microorganisms in biological wastewater treatment systems. Water Res 43:3177–3186CrossRefGoogle Scholar
  43. Pant HH, Rao MV (2010) Evaluation of in vitro anti-genotoxic potential of melatonin against arsenic and fluoride in human blood cultures. Ecotoxicol Environ Saf 73:1333–1337CrossRefGoogle Scholar
  44. Pinheiro MAA, Duarte LFA, Toledo TR, Adam ML, Torres RA (2013) Habitat monitoring and genotoxicity in Ucides cordatus (Crustacea: Ucididae), as tools to manage a mangrove reserve in southeastern Brazil. Environ Monit Assess 185:8273–8285CrossRefGoogle Scholar
  45. Podder S, Chattopadhyay A, Bhattacharya S, Ray MR, Chakraborty A (2010) Fluoride induced genotoxicity in mouse bone marrow cells: effect of buthionine sulfoximine and N-acetyl cysteine. J Appl Toxicol 7:618–625Google Scholar
  46. Podder S, Chattopadhyay A, Bhattacharya S (2011) Reduction in fluoride-induced genotoxicity in mouse bone marrow cells after substituting high fluoride-containing water with safe drinking water. J Appl Toxicol 31(7):703–705CrossRefGoogle Scholar
  47. Poulsen R (2011) The effect of fluoride pollution on soil microorganisms. Thesis in partial fulfilment of a Baccalaureus Scientiarum degree in biochemistry. University of Iceland, Reykjavik, p 42Google Scholar
  48. Rocco L, Frenzilli G, Fusco D, Peluso C, Stingo V (2010) Evaluation of zebrafish DNA integrity after exposure to pharmacological agents present in aquatic environments. Ecotoxicol Environ Saf 73:1530–1536CrossRefGoogle Scholar
  49. Sadiq MI, Chowdhury B, Chandrasekaran N, Mukherjee A (2009) Antimicrobial sensitivity of Escherichia coli to alumina nanoparticles. Nanomed Nanotechnol Biol Med 5:282–286CrossRefGoogle Scholar
  50. Schmid W (1976) The micronucleus test for cytogenetic analysis. In: Hollander A (ed) Chemical mutagens 4. Plenum Press, New York, pp 31–53CrossRefGoogle Scholar
  51. Sellami I, Guermazi W, Hamza A, Aleya L, Ayadi H (2010) Seasonal dynamics of zooplankton community in four Mediterranean reservoirs in humid areas (Beni Mtir: north of Tunisia) and semi-arid area (Lakhmes, Nabhana and Sidi Saâd: center of Tunisia). J Therm Biol 25:392–400CrossRefGoogle Scholar
  52. Seukep J, Noumedem JAK, Djeussi DE, Kuete V (2014) Genotoxicity and teratogenicity of African medicinal plants. In: Kuete V (ed) Toxicol Survey of African Medicinal Plants, Elsevier, p 235–275Google Scholar
  53. Shugart LR, Theodorakis C (1996) Genetic ecotoxicology: the genotypic diversity approach. Comp Biochem Physiol C 113:273–276Google Scholar
  54. Tamokou JD, Kuete V (2014) Mutagenicity and carcinogenicity of African medicinal plants. In: Kuete V (Ed) Toxicological survey of African medicinal Plants. pp 277–322Google Scholar
  55. Tiwari H, Rao MV (2010) Curcumin supplementation protects from genotoxic effects of arsenic and fluoride. Food Chem Toxicol 48:1234–1238CrossRefGoogle Scholar
  56. Torres de Lemos C, de Almeida Iranço F, D'Ávila de Oliveira NC, Dornelles de Souza G, Guimarães Fachel JM (2008) Biomonitoring of genotoxicity using micronuclei assay in native population of Astyanax jacuhiensis (Characiformes: Characidae) at sites under petrochemical influence. Sci Total Environ 406:337–343CrossRefGoogle Scholar
  57. Walker GC (1987) The SOS response of E.coli. In: Neidhardt JC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington DC, pp 1346–1357Google Scholar
  58. Watanabe H, Kobayashi K, Kato Y, Oda S, Abe R, Tatarazako N, Iguchi T (2008) Genomic response in Daphnia to chemical pollutants. In: Murakami Y, Nakayama K, Kitamura SI, Iwata H, Tanabe S (eds) Interdisciplinary studies on environmental chemistry, vol 1. Biological Responses to Chemical Pollutants, Terrapub, Tokyo, pp 133–142Google Scholar
  59. Zouabi Aloui B, Gueddari M (2009a) Long-term water quality monitoring of the Sejnane reservoir in Northeast Tunisia. Bull Eng Geol Environ 68:307–316CrossRefGoogle Scholar
  60. Zouabi Aloui B, Gueddari M (2009b) A multivariate assessment of the trophic state of a man-made reservoir in North Tunisia. Limnol Rev 13(4):229–240CrossRefGoogle Scholar
  61. Zouabi Aloui B, Gueddari M (2013) A multivariate assessment of the trophic state of a man-made reservoir in North Tunisia. Limnol Rev 13(4):229–240Google Scholar
  62. Zouabi Aloui B, Adelana SM, Gueddari M (2015) Effects of selective withdrawal on hydrodynamics and water quality of a thermally stratified reservoir in the southern side of the Mediterranean Sea: a simulation approach. Environ Monit Assess 187:292–311CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zouhour Ouanes-Ben Othmen
    • 1
    Email author
  • Sabria Barka
    • 1
  • Zied Ben Adeljelil
    • 2
  • Samia Mouelhi
    • 3
  • Mounira Krifa
    • 4
  • Soumaya Kilani
    • 4
  • Leila Chekir-Ghedira
    • 4
  • Joëlle Forget-Leray
    • 5
  • Amel Hamza-Chaffai
    • 1
  1. 1.Unité de Recherche de Toxicologie Environnementale et Marine, UR 09-03IPEIS Sfax UniversitySfaxTunisia
  2. 2.Biochemistry Laboratory-Medicine Faculty of Monastir: LR12ES05Monastir UniversityMonastirTunisia
  3. 3.Unité de Recherche de Biologie Animale et Systématique Evolutive 2092, Faculté des Sciences de TunisCampus Universitaire Manar IITunisTunisia
  4. 4.Unité de Recherche de Pharmacognosie/Biologie Moléculaire 99/UR/07-03, Faculté de PharmacieMonastir UniversityMonastirTunisia
  5. 5.Laboratoire d’Ecotoxicologie des Milieux Aquatiques, EA 3222, FED 4116 SCALEUniversité du HavreLe HavreFrance

Personalised recommendations